Electronic Supplementary Material

Lambertz M, Grommes K, Kohlsdorf T, Perry SF. 2015. Lungs of the first amniotes: why simple if they can be complex?
Biology Letters 11, 20140848. doi:10.1098/rsbl.2014.0848
Electronic Supplementary Material
1. Material and Methods
Specimens for dissection were obtained from different institutions and private keepers (see
detailed list below). Animals either were frozen (fr), preserved in ethanol (EtOH), or fixed in
formaldehyde (FA).
Institutional abbreviations are as follows:
CHRP
Coleção Herpetológica de Ribeirão Preto (Ribeirão Preto, Brazil)
CHUNB Coleção Herpetológica da Universidade de Brasília (Brasília, Brazil)
MNHN
Muséum national d'histoire naturelle (Paris, France)
UCMZ
University of Calgary Museum of Zoology (Calgary, Canada)
ZFMK
Zoologisches Forschungsmuseum Alexander Koenig (Bonn, Germany)
ZSM
Zoologische Staatssammlung München (Munich, Germany)
The total number of specimens per species examined, as well as state of preservation, are
indicated in the taxonomic list below. Accession numbers are provided where specimens are
deposited in official collections, otherwise they are labelled as coming from a private
collection (priv). Snout­vent length (SVL), measured with callipers (to the nearest 0.1 mm)
or measuring tape (to the nearest 0.5 mm), is provided as a standard measurement.
The coelomic cavity of the specimens was dissected ventrally and the lungs were removed
carefully. In several instances the lungs of previously frozen specimens first were filled in
situ with 4% formaldehyde (w/v) and fixed in an inflated state. When necessary, dissections
were performed under a stereoscopic dissecting microscope.
The excised lungs of most reptiles were filled upon removal with aqueous alcoholic dilutions
(ethanol) beginning with 70% (v/v) and successively dehydrated by submersion in and filling
of the lungs, ending at 100% ethanol. Dehydrated lungs were dried under a constant air
flow. For this purpose, a blunt cannula was inserted into either the trachea or
extrapulmonary bronchus and fixed with a cable tie. An aquarium air pump (Schego WS2,
Schemel & Goetz GmbH & Co. KG, 63069 Offenbach am Main, Germany) provided air flow,
which was adjusted as needed by a valved exit branch. The dried lungs were cut open with
fine scissors and razor blades to reveal the internal structure.
All photographs were made with a digital single lens reflex camera (Canon EOS 5D Mark
II) and varying standard lenses (Canon Zoom Lens EF 24­105mm 1:4L IS, Canon Macro
Lens EF 100mm 1:2.8L IS, Canon Lens EF 50mm 1:1.8) or a Zeiss TESSOVAR
Photomacrographic Zoom System.
The dried tuatara lung was scanned with a v|tome|x s µCT device (GE Sensing &
Inspection Technologies GmbH, phoenix|x­ray, Wunstorf, Germany) at the Steinmann­
Institut für Geologie, Mineralogie und Paläontologie, Bereich Paläontologie, Rheinische
Friedrich­Wilhelms­Universität Bonn (Germany) with a resolution of 69.57 µm per voxel
and visualized using VGStudio MAX 2.0 software (Volume Graphics GmbH, Heidelberg,
Germany).
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Lambertz M, Grommes K, Kohlsdorf T, Perry SF. 2015. Lungs of the first amniotes: why simple if they can be complex?
Biology Letters 11, 20140848. doi:10.1098/rsbl.2014.0848
For mammals and birds, airway casts were obtained by filling the lungs in situ with a
silicone elastomer (Dow Corning 734), which was diluted by admixture of 10% (v/v) low­
viscosity silicone oil. The lungs were then removed and the tissue was macerated in 6%
sodium hypochlorite in order to obtain a cast of the intrapulmonary airways. Details on this
method are published by Perry et al. [24].
The animal material used in this study for the embryological analysis was obtained in
accordance with German animal protection law, § 4, Abs. 1 and 3 of the Tierschutzgesetz
(Tierschutzgesetz in der Fassung der Bekanntmachung vom 18. Mai 2006 (BGBI. I S. 1206,
1313), last amendment: Artikel 20 des Gesetzes vom 9. Dezember 2010 (BGBI. I S. 1934)).
Embryos at different developmental stages (approximately between 10 days post­oviposition
[dpo] and 50 dpo, compare also Noro et al. [25]) were killed with MS­222 at a concentration
of 5 g/l and dissected free from the surrounding extraembryonic tissue in phosphate­
buffered saline (PBS) (0.1M, pH 7.4). They were afterwards fixed in 4%
paraformaldehyde/PBS (w/v) for at least 24 hours. Lungs were removed from the specimens
while submersed in PBS. All dissections were performed under a stereoscopic dissecting
microscope. Developmental stages of P. picta lungs were analysed in PBS and imaged using
a Canon EOS 5D Mark II digital single lens reflex camera mounted on a Zeiss TESSOVAR
Photomacrographic Zoom System and a Schott KL 1500 illuminant adjusted to a spectral
regime of 540 nm.
2. List of taxa examined
2.1. Lepidosauria – Lizards and Snakes
2.1.1. Amphisbaenia
2.1.1.1. Amphisbaenidae
Amphisbaena hastata VANZOLINI, 1991: CHRP 317, 331, 332, 333 [4, FA], SVL: 116­170 mm
2.1.2 Anguimorpha
2.1.2.1. Anguidae
Anguis fragilis LINNAEUS, 1758: priv [1, EtOH], SVL: 155 mm
Ophiodes cf. striatus (SPIX, 1824): CHUNB 52393, 57515 [2, EtOH], SVL: 178­210 mm
2.1.2.2. Helodermatidae
Heloderma horridum (WIEGMANN, 1829): priv [1, fr], SVL: 349 mm
2.1.2.3. Varanidae
Varanus acanthurus (BOULENGER, 1885): priv [2, fr], SVL: 66­144 mm
V. macraei BÖHME & JACOBS, 2001: priv [1, fr], SVL: 316 mm
2.1.3. Gekkota
2.1.3.1. Eublepharidae
Eublepharis macularius (BLYTH, 1854): ZFMK uncat., priv [3, fr, EtOH], SVL: 106­116 mm
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Lambertz M, Grommes K, Kohlsdorf T, Perry SF. 2015. Lungs of the first amniotes: why simple if they can be complex?
Biology Letters 11, 20140848. doi:10.1098/rsbl.2014.0848
2.1.3.2. Gekkonidae
Paroedura picta (PETERS, 1854): priv [1, fr], SVL: 59 mm
Phelsuma madagascariensis GRAY, 1831: priv [1, EtOH], SVL: 70.5 mm
2.1.3.3. Pygopodidae
Lialis burtonis GRAY, 1835: priv [1, fr], SVL: 226 mm
2.1.4. Iguania
2.1.4.1. Agamidae
Chlamydosaurus kingii GRAY, 1825: priv [1, fr], SVL: 164 mm
Pogona barbata (CUVIER, 1829): priv [2, fr], SVL: 193­202 mm
2.1.4.2. Chamaelionidae
Trioceros rudis (BOULENGER, 1906): priv [1, fr], SVL: 77 mm
2.1.4.3. Dactyloidae
Anolis auratus DAUDIN, 1802: CHUNB 07776, 07877, 07880 [3, EtOH], SVL: 42­42.5 mm
A. fuscoauratus D'ORBIGNY, 1837: CHUNB 22818, 22820 [2, EtOH], SVL: 45.5­47 mm
A. punctatus DAUDIN, 1802: CHUNB 47010, 47014 [2, EtOH], SVL: 71.5­81 mm
Norops nitens (WAGLER, 1830): CHUNB 58055, 58060, 58063 [3, EtOH], SVL: 58­64.5 mm
2.1.4.4. Hoplocercidae
Hoplocercus spinosus FITZINGER, 1843: CHUNB 05291, 05296, 05299 [3, EtOH], SVL: 81­106 mm
2.1.4.5. Iguanidae
Iguana iguana (LINNAEUS, 1758): CHUNB 58266 [1, EtOH], SVL: 240 mm
2.1.4.6. Leiosauridae
Enyalius sp.: CHUNB 38190, 29311, 29312, 29294 [4, EtOH], SVL: 67.5­78 mm
Enyalius aff. bilineatus (DUMÉRIL & BIBRON, 1837): CHUNB 29316 [1, EtOH], SVL: 68.5 mm
2.1.4.7. Liolaemidae
Liolaemus lutzae MERTENS, 1938: CHUNB 13727, 30475, 42589 [3, EtOH], SVL: 47.5­66 mm
2.1.4.8. Phrynosomatidae
Phrynosoma cornutum (HARLAN, 1824): UCMZ­R 1975­63, 1975­239 [2, EtOH], SVL: 87 mm
P. hernandesi GIRARD, 1858: UCMZ­R 1974­064, 1986­11 [2, EtOH], SVL: 76 mm
Sceloporus cf. occidentalis BAIRD & GIRARD, 1852: UCMZ­R 1982­1­20 [2, EtOH], SVL: 65­71 mm
2.1.4.9. Polychrotidae
Polychrus acutirostris SPIX, 1825: CHUNB 47413, 47414, 47418, 47419 [4, EtOH],
SVL: 114.5­123 mm
P. marmoratus (LINNAEUS, 1758): CHUNB 57383, 57387 [2, EtOH], SVL: 112­139 mm
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Lambertz M, Grommes K, Kohlsdorf T, Perry SF. 2015. Lungs of the first amniotes: why simple if they can be complex?
Biology Letters 11, 20140848. doi:10.1098/rsbl.2014.0848
2.1.4.10. Tropiduridae
Eurolophosaurus amathites (RODRIGUES, 1984): CHRP 267, 269­273 [6, EtOH],
SVL: 60.5­75 mm, see [26]
E. divaricatus (RODRIGUES, 1986): CHRP 297, 300, 306, 314­316 [6, EtOH],
SVL: 66.5­91.5 mm, see [26]
Plica plica (LINNAEUS, 1758): CHUNB 10112, 10113, 10117 [3, EtOH], SVL: 89­111 mm
P. umbra (LINNAEUS, 1758): CHUNB 10122, 10126, 22545 [3, EtOH], SVL: 60­92.5 mm
Stenocercus caducus (COPE, 1862): CHUNB 49267 [1, EtOH], SVL: 66.5 mm
S. sinesaccus TORRES­CARVAJAL, 2005: CHUNB 18048, 18049 [2, EtOH], SVL: 71­76 mm
Tropidurus hygomi REINHARDT & LÜTKEN, 1861: CHRP 473, 475, 476, 479­481 [6, EtOH],
SVL: 60­69.9 mm, see [26]
T. psammonastes RODRIGUES et al., 1988: CHRP 320­325 [6, EtOH], SVL: 89.5­97.5 mm, see [26]
Uranoscodon superciliosus (LINNAEUS, 1758): CHUNB 10106, 10107 [2, EtOH],
SVL: 136.5­140 mm
2.1.5. Rhynchocephalia
2.1.5.1. Sphenodontidae
Sphenodon punctatus (GRAY, 1842): ZSM 1318/2006 [1, EtOH], SVL: 192 mm
2.1.6. Scincomorpha
2.1.6.1. Cordylidae
Cordylus sp.: priv [1, fr], SVL: 98 mm
2.1.6.2. Gymnophthalmidae
Calyptommatus leiolepis RODRIGUES, 1991: CHRP 334, 335, 336, 340, 341, 342 [6, FA],
SVL: 44.5­57 mm
Vanzosaura multiscutatus (AMARAL, 1933): CHRP 337, 338, 339, 343, 344, 345 [6, FA],
SVL: 26.5­36 mm
2.1.6.3. Teiidae
Ameiva ameiva (LINNAEUS, 1758) ­ priv [2, FA], SVL: 93­144 mm
Salvator merianae DUMÉRIL & BIBRON, 1839: priv [2, FA], SVL: 107­108 mm
2.1.6.4. Scincidae
Chalcides sp.: priv [1, EtOH], SVL: 80 mm
Corucia zebrata GRAY, 1855: priv [1, fr], SVL: 126 mm
Mabuya sp.: ZFMK uncat. [1, EtOH], SVL: 75 mm
Tribolonotus gracilis DE ROOIJ, 1909: ZFMK uncat [1, EtOH], Svl: 101 mm
2.1.7. Serpentes
2.1.7.1. Achrochordidae
Acrochordus javanicus HORNSTEDT, 1787: priv [1, fr], SVL: 630 mm
2.1.7.2. Boidae
Eryx colubrinus (LINNAEUS, 1758): priv [2, fr, FA], SVL: 219­276 mm
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Lambertz M, Grommes K, Kohlsdorf T, Perry SF. 2015. Lungs of the first amniotes: why simple if they can be complex?
Biology Letters 11, 20140848. doi:10.1098/rsbl.2014.0848
2.1.7.3. Dipsadidae
Apostolepis gaboi RODRIGUES, 1993: [1, EtOH], SVL: 315 mm
2.1.7.4. Elapidae
Aspidelaps lubricus (LAURENTI, 1768): priv [1, FA], SVL: 496 mm
Naja kaouthia LESSON, 1831: priv [2, FA], SVL: 1065­1140 mm
N. pallida BOULENGER, 1896: priv [5, FA], SVL: 621­1230 mm
N. siamensis LAURENTI, 1768: priv [1, FA], SVL: 810 mm
2.1.7.5. Pythonidae
Python regius (SHAW, 1802): priv [4, fr, FA], SVL: 167­1113 mm
2.1.7.6. Typhlopidae
Afrotyphlops lineolatus (JAN, 1864): priv [1, fr], SVL: 270 mm
2.1.7.7. Viperidae
Bitis arietans (MERREM, 1820): priv [1, FA], SVL: 662 mm
Crotalus atrox BAIRD & GIRARD, 1853: priv [3, fr, FA], SVL: 232­ 756 mm
2.2. Crocodylia – Crocodiles
2.2.1. Alligatoridae
Alligator mississippiensis (DAUDIN, 1802): priv [1, fr], SVL: 580 mm
Caiman crocodilus (LINNAEUS, 1758): priv [1, FA], SVL: 167 mm
2.3. Testudines – Turtles
2.3.1. Chelydridae
Chelydra serpentina (LINNAEUS, 1758): 5 adult specimens, see [23]
Macrochelys temminckii (TROOST in HARLAN, 1835): 1 adult specimen, see [23]
2.3.2. Emydidae
Trachemys scripta (THUNBERG in SCHOEPFF, 1792): 4 adult specimens, see [23]
2.3.3. Kinosternidae
Sternotherus carinatus (GRAY, 1856): ZSM 438­439/2001 [2, EtOH]
2.3.4. Platysternidae
Platysternon megacephalum GRAY, 1831: 6 adult specimens, see [23]
2.3.5. Testudinidae
Testudo hermanni GMELIN, 1789: 4 adult specimens, see [23]
2.4. Aves – Birds
2.4.1. Columbiformes
2.4.1.1. Columbidae
Columba domestica GMELIN, 1789: 3 adult [fr] specimens
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Lambertz M, Grommes K, Kohlsdorf T, Perry SF. 2015. Lungs of the first amniotes: why simple if they can be complex?
Biology Letters 11, 20140848. doi:10.1098/rsbl.2014.0848
2.4.2. Galliformes
2.4.2.1. Phasianidae
Gallus domesticus GMELIN, 1789: 3 adult specimens, see [27]
2.5. Mammalia – Mammals
2.5.1. Rodentia
2.5.1.1. Muridae
Mus musculus LINNAEUS, 1758: 5 adult [fr] specimens
Rattus norvegicus (BERKENHOUT, 1769): 4 adult [fr] specimens
2.6. Lissamphibia – Amphibians
2.6.1. Anura
2.6.1.1. Pipidae
Xenopus laevis (DAUDIN, 1802): 3 adult [EtOH, FA] specimens
2.6.1.2. Ranidae
Lithobates catesbeianus (SHAW, 1802): 6 adult [EtOH] specimens, see [28]
2.6.2. Caudata
2.6.2.1. Cryptobranchidae
Andrias japonicus (TEMMINCK, 1836): MNHN A, 1 historical specimen (lungs only) on display
2.6.2.2. Proteidae
Necturus maculosus (RAFINESQUE, 1818): 4 adult [FA] specimens
3. Lungs of the adult Madagascar ground gecko, Paroedura picta
The lungs of adult P. picta (figure S2) closely resemble those of the later developmental
stages of this species: there is no significant post­hatching modification of the anatomical
lung structure. The only one evident involves the continued dilation and general increase in
pulmonary size and the left lung is smaller than the right one, as it is frequently observed
in lepidosaurian lungs.
Externally, the pulmonary artery is clearly visible and enters the lung together with the
subapically entering bronchus. The subapical bronchial and arterial entrances define the
posterior margin of a discrete apical region (apical “chamber”). Internally, the lungs
constitute a typical lepidosaurian single­chambered lung, which is characterized by small
septa forming dorsomedial and ventrolateral niches. These niches are also supplied by
individual branches of the pulmonary artery.
4. The lungs of monitor lizards
Varanoids represent the only example among lepidosaurs that exhibit true multichambered
lungs. Unfortunately, embryological data on pulmonary development that would allow us to
directly compare developmental stages are lacking for this taxon, but the Madagascar
ground gecko ontogenetically demonstrates a sequential array of discrete dorsal and ventral
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Lambertz M, Grommes K, Kohlsdorf T, Perry SF. 2015. Lungs of the first amniotes: why simple if they can be complex?
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chamber­like elements that strikingly resemble the chambers in the adult monitor lung
(figure S3). Whereas in the gecko the central lumen becomes dilated during later
development, obscuring the initial branched structure (figures 1 and S2), the monitor
apparently uses this ontogenetic stage as a template for its multichambered lungs.
5. Ancestral state reconstructions of pulmonary characters among amniotes
We used our new comparative anatomical and embryological data to perform ancestral state
reconstructions using Mesquite Version 2.74 [8]. Ancestral reconstructions were performed
using parsimony; character states were unordered. The topology adopted consisted of an
ultrametrized tree based on Pyron et al. [29] for a “family”­level lepidosaur approach and
Field et al. [30] for an amniote­wide approach. We ran the analyses separately for the
following two character complexes. The first data set comprises two character states of
pulmonary anatomy based on developmental trajectory: (0) lungs forming a tube that
expands into a sac, which remains as such in the adult, or (1) lungs forming a tube that
sequentially produces discrete buds, which remain traceable in the adult lung either as
smaller septa or larger chambers/bronchi. The second data set refers to the pulmonary
vasculature, and also was coded for two character states: (0) the pulmonary artery forms a
plexus that envelopes the entire lung, or (1) the pulmonary artery forms in a strictly
hierarchically branched pattern that coincides with internal pulmonary structures (septa or
chambers/bronchi).
These analyses (figures S4­5) revealed that for both characters the “complex” state (coded as
1) was probably ancestral to the lineage; the two approaches (the lepidosaur and the
amniote­wide) provide evidence for such basal conditions of complex states. The principal
pulmonary branching as well as the hierarchically branching pulmonary artery are both
shared as derived character states by all amniotes including lepidosaurs. These analyses
thereby provide statistical support for our hypothesis that amniote lungs exhibited
complexity at the lineage’s origin and that the simplicity observed in most adult lepidosaurs
is a secondary phenomenon.
6. References
24. Perry SF, Purohit AM, Boser S, Mitchell I, Green FHY. 2000. Bronchial casts of human
lungs using negative pressure injection. Exp. Lung Res. 26, 27­39.
25. Noro M, Uejima A, Abe G, Manabe M, Tamura K. 2009. Normal developmental stages of
the Madagascar ground gecko Paroedura pictus with special reference to limb
morphogenesis. Dev. Dyn. 238, 100­109.
26. Lambertz M, Kohlsdorf T, Perry SF, Ávila RW, da Silva RJ. 2012. First assessment of
the endoparasitic nematode fauna of four psammophilous species of Tropiduridae
(Squamata: Iguania) endemic to north­eastern Brazil. Acta Herpetologica 7, 315­323.
27. Sverdlova NS, Lambertz M, Witzel U, Perry SF. 2012. Boundary conditions for heat
transfer and evaporative cooling in the trachea and air sac system of the domestic fowl: a
two­dimensional CFD analysis. PLoS ONE 7, e45315.
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Lambertz M, Grommes K, Kohlsdorf T, Perry SF. 2015. Lungs of the first amniotes: why simple if they can be complex?
Biology Letters 11, 20140848. doi:10.1098/rsbl.2014.0848
28. Lambertz M, Schmied H. 2010. An ingrown ground beetle in the middle ear cavity of a
North American bullfrog, Lithobates catesbeianus. Salamandra 46, 185­186.
29. Pyron RA, Burbrink FT, Wiens JJ. 2013. A phylogeny and revised classification of
Squamata, including 4161 species of lizards and snakes. BMC Evol. Biol. 13, 93.
30. Field DJ et al. 2014. Toward consilience in reptile phylogeny: miRNAs support an
archosaur, not lepidosaur, affinity for turtles. Evol. Dev. 16, 189­196.
31. Moser F. 1902. Beiträge zur vergleichenden Entwicklungsgeschichte der
Wirbeltierlunge. (Amphibien, Reptilien, Vögel, Säuger). Archiv für Mikroskopische
Anatomie und Entwicklungsgeschichte 60, 587­668 + Pls. XXX­XXXIII.
32. Hesser C. 1905. Über die Entwickelung der Reptilienlungen. Anatomische Hefte, I.
Abtheilung 29, 215­310 + Pls. 19­29.
33. Broman I. 1942. Über die Embryonalentwicklung der Chamäleonlungen. Gegenbaurs
Morphol. Jahrb. 87, 490­535.
34. Milani A. 1894. Beiträge zur Kenntniss der Reptilienlunge. Zool. Jahrb. (Abt. Anat.
Ontog. Tiere) 7, 545­592 + Pls. 30­32.
Figure S1. Early developmental stages of lungs in various tetrapods.
(a) Neither structural similarity nor a blood vessel pattern that could reveal even a
transient existence of a subapical bronchial entrance is observed in any of the amphibian
lungs. They originate as an unstructured tube and dilate to eventually become “sac­like”,
despite the presence of septate parenchyma. The airway enters the lungs at their anterior­
most point (apical entrance), as does the pulmonary artery. All illustrations after [31]. (b)
All of the lepidosaurs show at least a cranial bud of the lung that overgrows the bronchial
entrance. However, there are further indications of a sequential formation of additional
branches, which during development become obscured and persist in the adult as small
septa. Sphenodon, Anguis and Podarcis after [31], Cnemidophorus after [32], Trioceros after
[33]. (c) Note that the basic branching pattern not only shows remarkable congruence
among these distantly related non­lepidosaurian amniote taxa, but also is reminiscent of the
early developmental stages in lepidosaurs exhibiting simpler lung types. Chrysemys after
[15], Alligator after [16], Gallus after [17], Mus after [14].
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Lambertz M, Grommes K, Kohlsdorf T, Perry SF. 2015. Lungs of the first amniotes: why simple if they can be complex?
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Figure S2. Dried lungs of an adult Paroedura picta.
Left lung in exterior lateral view on the left, and right lung in internal medial view on the
right. Anterior is to the left in both illustrations. The apical “chamber” and the septa that
form the borders of the dorsomedial and ventrolateral niches are indicated by white lines.
Note further that the course of the pulmonary artery follows exactly the posterior border of
the apical “chamber”, and that also the bordering septa of the dorsomedial and ventrolateral
niches are each supplied by hierarchical branches of the pulmonary artery.
Figure S3. Developing gecko lung vs. adult monitor lizard lung.
Despite the fundamental difference of the adult gecko lung to that of the monitor, the early
developmental stage shows a remarkable structural congruence. Schematic diagram of the
monitor lung after [34].
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Lambertz M, Grommes K, Kohlsdorf T, Perry SF. 2015. Lungs of the first amniotes: why simple if they can be complex?
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Figure S4. The ancestral pulmonary Bauplan of lepidosaurs.
The ancestral state reconstructions reveal that pulmonary branching during early
development is a shared derived trait of all lepidosaurs. The same applies to the branching
pattern of the pulmonary artery (not shown).
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Lambertz M, Grommes K, Kohlsdorf T, Perry SF. 2015. Lungs of the first amniotes: why simple if they can be complex?
Biology Letters 11, 20140848. doi:10.1098/rsbl.2014.0848
Figure S5. The ancestral pulmonary Bauplan of amniotes.
The ancestral state reconstructions reveal that pulmonary branching during early
development is a shared derived trait of all amniotes. In comparison with the traditional
interpretation where each complex type of lung evolved independently among amniotes
(left), our new hypothesis of an initial presence of complexity (right) involves substantially
fewer evolutionary steps. The sa applies to the hierarchical branching pattern of the
pulmonary artery (not shown).
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